Effect of Feed Restriction and Photoperiod on Reproduction and LEPR, MELR mRNA Expression of Layers

E HAO H Chen S Ge R Huang About the authors

ABSTRACT

Photoperiod and nutrition are major factors that affect the reproductive efficiency particularly in female animals. In this study we examined the interaction of photoperiod and food restriction on growth, sexual maturation and receptor mRNA expressions of leptin, melatonin, and estrogen in abdominal fat and the ovary of pullets. There were no interaction effects between photoperiod and feeding level on body weight, abdominal fat weight, ovary weight at both 14 wk and 18 wk. Abdominal fat weight of feed restriction group was significantly lower compared with the control group at the age of 14 wk, 18 wk, and age of the first egg (AFE) (p<0.05). Ovary LEPR (Leptin receptor) gene expression showed an interaction effect of the first egg. Restricted feeding significantly inhibited ovary ER (Estrogen receptor), LEPR and MELR1B (Melatonin 1B receptor) gene expression at 14 wk, 18 wk and the first egg. At 14-week-old, abdominal fat LEPR gene expression was significantly lower in long photoperiod group compared with the short photoperiod group. At the first egg, short photoperiod and feed restriction group reduced abdominal fat LEPR gene expression. The results indicated that the reproductive activity of pullets is sensitive to feed intake and photoperiod. Feed restriction down regulated the ER, LEPR, MELR1A (Melatonin 1A receptor) and MELR1B mRNA expression of the ovary at 14 wk, 18wk and AFE. Long photoperiod enhanced the LEPR, MELR1A and MELR1B mRNA expression of abdominal fat at AFE.

Keywords:
Feed restriction; MELR; Ovary; Photoperiod; Pullet

INTRODUCTION

Laying hens, like many other birds, rely heavily on vision, and light is an important factor within their natural environment (Huber-Eicher et al., 2013Huber-Eicher, B, Suter, A, Spring-Stã¤Hli, P, 2013. Effects of colored light-emitting diode illumination on behavior and performance of laying hens. Poult Sci,92(4):869-873.). Lighting is the factor that most affects the performance of the production and reproduction of birds, sexual maturation, feeding behavior and productivity of eggs and egg weight (Lewis et al., 2010; Lewis Gous, 2006; Schweanlardner et al., 2012Schweanlardner,K, Fancher BI, Classen HL. Impact of daylength on the productivity of two commercial broiler strains. British Poultry Science 2012;53(1):7-18.). Nutrition is another major factor that affects the reproductive efficiency particularly in female animals (Brecchia et al., 2006Brecchia G, Bonanno A, Galeati G, Federici C, Maranesi M, Gobbetti A, et al. Hormonal and metabolic adaptation to fasting:effects on the hypothalamic-pituitary-ovarian axis and reproductive performance of rabbit does. Domestic Animal Endocrinology 2006;31(2):105-122.; Walzem Chen, 2014Walzem RL, Chen S. Obesity-induced dysfunctions in female reproduction:lessons from birds and mammals. Advances in Nutrition: An International Review Journal 2014;5(2):199-206.). Various nutritional methods have been employed in breeder pullets for attempting to reduce body weight at the onset of egg laying in order to improve performance during the laying period (Bozkurt et al., 2014Bozkurt M, Ayhan V, Kirkpinar F. The effects of different qualitative and quantitative feed restriction methods during rearing on the reproductive performance of broiler breeder hens. Revue De Médecine Vétérinaire 2014;163(8):405-410.; De Coon, 2007; Proudfoot, 1979Proudfoot FG. Effect of rearing and adult feed restriction and photoperiod regimens on the performance of four meat parent chicken genotypes. Canadian Journal of Animal Science 1979;59(4):749-759.). Feed restriction has been justified as a means of controlling body weight, improving subsequent reproduction to achieve greater production efficiency without inflicting severe adverse effects on the birds’ nutritional requirements (Crouch et al., 2002Crouch AN, Grimes JL, Christensen VL, Krueger KK. Effect of physical feed restriction during rearing on Large White turkey breeder hens:2. reproductive performance. Poultry Science 2002;81(1):16-22.; De Coon, 2007; Hocking, 2004Hocking PM. Roles of body weight and feed intake in ovarian follicular dynamics in broiler breeders at the onset of lay and after a forced molt. Poultry Science 2004;83(12):2044-2050.). Photoperiod cues plays important roles in the regulation of seasonal variations in body mass (BM) and energy balance for many small mammals (Zhao & Wang, 2006).

Leptin, a 146-amino acid protein, is mainly secreted by adipocytes (Paczoska-Eliasiewicz et al., 2006Paczoska-Eliasiewicz HE, Proszkowiec-Weglarz M, Proudman J, Jacek T, Mika M, Sechman A, et al. Exogenous leptin advances puberty in domestic hen. Domestic Animal Endocrinology 2006;31(3):211-226.; Sirotkin & Grossmann, 2015Sirotkin AV, Grossmann R. Interrelationship between feeding level and the metabolic hormones leptin, ghrelin and obestatin in control of chicken egg laying and release of ovarian hormones. Comparative Biochemistry and Physiology Part A:Molecular & Integrative Physiology 2015;184(1-5).) and is implicated in the regulation of metabolic status, feed intake, reproduction, immune function and body condition in rodent and primates (Bouloumie et al., 1998Bouloumie A, Drexler HC, Lafontan M, Busse R. Leptin, the product of Ob gene, promotes angiogenesis. Circulation Research 1998;83(10):1059-1066.; Fantuzzi & Faggioni, 2000Fantuzzi G, Faggioni R. Leptin in the regulation of immunity, inflammation, and hematopoiesis. Journal of Leukocyte Biology 2000;68(4):437-446.; Zieba et al., 2005Zieba DA, Amstalden M, Williams GL. Regulatory roles of leptin in reproduction and metabolism: a comparative review. Domestic Animal Endocrinology 2005;29(1):166-185.). Gallus Gallus leptin cDNA was first cloned by Taouis (Taouis et al., 1998Taouis M, Chen JW, Daviaud C, Dupont J, Derouet M, Simon J. Cloning the chicken leptin gene. Gene 1998;208(2):239-242.), which led to a controversy whether a leptin gene exists in the chicken genome (Pitel et al., 2010Pitel F, Faraut T, Bruneau G, Monget P. Is there a leptin gene in the chicken genome? Lessons from phylogenetics, bioinformatics and genomics. General and Comparativo Endocrinology 2010;167(1):1-5.). Although the sequence of the chicken leptin gene is controversial, cloning of the chicken leptin receptor gene provides evidence of the existence of the leptin homologue in birds (Horev et al., 2000Horev G, Einat P, Aharoni T, Eshdat Y, Friedman-Einat M. Molecular cloning and properties of the chicken leptin-receptor (CLEPR) gene. Molecular and Cellular Endocrinology 2000;162(1-2):95-106.; Liu et al., 2007Liu X, Dunn IC, Sharp PJ, Boswell T. Molecular cloning and tissue distribution of a short form chicken leptin receptor mRNA. Domestic Animal Endocrinology 2007;32(3):155-166.). Melatonin (N-acetyl-5-methoxytryptamine), an indole hormone, regulates circadian rhythm, hibernation, feeding pattern, thermoregulation, and neuroendocrine function in birds through three different receptor subtypes (MELR1A, MELR1b, and MELR1c) (Adachi et al., 2002Adachi A, Natesa, AK, Whitfield RMG, Weigum SE, Cassone, VM. Functional melatonin receptors and metabolic coupling in cultured chick astrocytes. Glia 2002;39(3):268-278.; Sinkalu et al., 2015Sinkalu VO, Ayo, JO, Abimbola AA, Ibrahim, JE. Effects of melatonin on cloacal temperature and erythrocyte osmotic fragility in layer hens during the hot-dry season. Journal of Applied Animal Research 2015;43(1):52-60.). In mammals, melatonin also influences the reproductive function via activation of receptor sites within the hypothalamic-pituitary-gonadal axis (Malpaux et al., 2001Malpaux B, Migaud M, Tricoire H, Chemineau P. Biology of mammalian photoperiodism and the critical role of the pineal gland and melatonin. Journal Biological Rhythms 2001;16(4):336-347.). In birds, melatonin binding sites have been identified in the ovaries, suggesting a possible role of melatonin regulating ovarian functions (Sundaresan et al., 2009Sundaresan NR, Marcus Leo MD , Subramani J, Anish D, Sudhagar M, Ahmed Ka, et al. Expression analysis of melatonin receptor subtypes in the ovary of domestic chicken. Veterinary Research Communications 2009;33(1):49-56.).

Following the attainment of minimum age and body weight thresholds, the present study was undertaken to investigate the relationship between photoperiod and feed restriction, and the possible mechanism about how the photoperiod, nutrition or both impact on the adipose store and the sexual maturity in pullets.

MATERIAL AND METHODS

Experimental Design, Birds, and Management

Female Gray Hy-line chicks were purchased from Hebei Huayu Poultry Breeding Company. Chicks were raised according to the management protocols established by Hy-line International. At 10 wk of age, 480 healthy pullets were selected and allotted randomly to one of the 6 treatments, i.e., a 3 (photoperiod: 8L:16D, 12L:12D, or 16L:8D) × 2 (ad libitum or feed restriction) factorial design. The feed restriction was 80% of the ad libitum. The diet contained 11.72 MJ/kg energy, 16.3% crude protein, 0.33% methionine and 0.74% lysine. The specific feeding and photoperiod schedule for the birds were given in Table 1. Each treatment had four replicates comprising 20 pullets each, 4 pullets per cage. Water was provided ad libitum throughout the study. Illumination was provided by 2 15-W compact fluorescent lamps producing a mean illuminance of 15 ± 2.4 lx. Pullets’ beaks were trimmed at 7 d of age, and all pullets were wing-banded at 6 wk. The present study was performed in accordance with Hebei Agricultural University Institutional Animal Care and Use Commit­tee Policies for Animal Use under an approved animal.

Table 1
Feeding and photoperiod treatments.

Sample Collection

Samples (n = 8 per feeding × photoperiod combi-nation) were collected at the age of 14 wk, 18 wk, and at first egg (AFE), respectively. Body weight was recorded, then pullets were killed by cervical dislocation. Weight of the abdominal fat (including the fat surrounding the gizzard) and the ovaries were measured, and then abdominal fat and ovaries were snap-frozen in liquid nitrogen, and stored at -80º until assayed. Also at the age of 18 wk, 2 pullets from each replicate were selected, weighed, and randomly placed in individual, illuminated, standard laying cages. The age and egg weight at first egg were recorded.

Isolation of Total mRNA and qPCR

Total RNA was isolated from the ovarian cortex and abdominal fat using the RNAeasy mini kit (Omega Bio-Tek, Inc.). Equal amounts of total RNA (1µg) were reverse transcribed into cDNA using the Reverse Transcription kit (TransGen Biotech, Inc). Amplification of specific transcripts was conducted using gene specific primers (Table 2). For each primer pair, only a single product of the predicted size was identified. All amplification products were sequenced to confirm specificity of the reaction. Abundance of specific mRNAs was analyzed by real -time PCR using the 2-ΔΔCt method (Livak Schmittgen, 2001Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2&lt; sup&gt;- ??CT&lt;/sup&gt; method. Methods 2001;25(4):402-408.). Values shown for transcript abundance are the Mean ± SEM.

Table 2
Primer sequences used for qPCR.

Statistical Analysis

The data were analyzed by two factors analyses of variance using the General Linear Models procedures of SPSS. When significant differences were determined for the main effects, comparison among means were made using the Duncan procedure. Unless otherwise stated, all statements of significance were assessed using p<0.05.

RESULTS

Body Weight, Ovary Weight and Abdominal Fat Weight

There were no interaction effects between photoperiod and feeding level on body weight, abdominal fat weight, and ovary weight at 14 wk, 18 wk, and at first egg (Table 3). However, treatment effects were detected. Abdominal fat weight of pullets from the feed restricted group was significantly lower compared with pullets from the ad libitum group at the age of 14wk, and AFE (p<0.05). Pullets’ ovary weight in the feed restricted group was lower compared to the ones in ad libitum group at the age of 14 wk (p<0.05). Lighting program effects were found on ovary weight at AFE only, it was lower in the 16L:8D group compared with the 12L:12D group but not the group of 8L:16D (p<0.01).

Table 3
Effect of feeding level and photoperiod on body weight, abdominal fat weight and ovary weight at the age of 14wk, 18wk, and AFE

Age of First Egg and First Egg Weight

There were no interaction effects between photoperiod and feed restriction on the age of the first egg and first egg weight (Table 4). However, long photoperiod significantly reduced the age of the first egg compared with the short photoperiod (p<0.05). The average age at the first egg was 146 d for the 16L:8D group and 156.45 d for the 8L:16D group. Photoperiod or feed restriction did not significantly affect the first egg weight (p>0.05).

Table 4
Effect of food restriction and photoperiod on age of first egg, and first egg weight.

LEPR, MELR1A, MELR1B Gene Expression

There were no photoperiod and feeding level interaction effects on abdominal fat LEPR, MELR1A, and MELR1B gene expression at 14 wk and 18 wk except LEPR at AFE (Table 5). At 14-week-old, abdominal fat LEPR and MELRIA gene expressions were significantly lower in the 16L:8D photoperiod group compared with the 8L:16D photoperiod group (p<0.05); feed restriction increased the abdominal fat LEPR expression compared with the ad libitum group at the age of 14 wk (p<0.05). However, at first egg, both LEPR and MELRIA gene expressions were higher in the 16L:8D long photoperiod group than in the 8L:16D short photoperiod (Table 5).

Table 5
Effect of food restriction and photoperiod on LEPR, MELR1A, MELR1B gene expression in abdominal fat of pullets.

There were also no photoperiod and feeding level interaction effects on the ovary ER, LEPR, MELR1A and MELR1B gene expression at 14 wk, 18 wk and first egg (Table 6). Feed Restriction significantly inhibited ovary ER, LEPR, MEIRIB, and MELR1B gene expression at 14 wk, 18 wk, and first egg, except MEIRIB at 18 wk . Photoperiod did not show significant differences on all measured genes at all the examined time periods (Table 6).

Table 6
Effect of food restriction and photoperiod on ER, LEPR, MELR1A, MELR1B gene expression in ovary of pullets.

DISCUSSION

It has been suggested that there is a BW or body composition threshold for the onset of sexual maturation (Brody et al., 1980Brody T, Eitan Y, Soller M, Nir I, Nitsan Z. Compensatory growth and sexual maturity in broiler females reared under severe food restriction from day of hatching. British Poultry Science 1980;21(6):437-446.; Brody et al., 1984). Chen (2007Chen H, Huang RL, Zhang HX, Di KQ, Pan D, Hou YG. Effects of photoperiod on ovarian morphology and carcass traits at sexual maturity in pullets. Poultry Science 2007;86(5):917-920.) reported that all lighting programs were effectively able to stimulate the sexual maturation process, however, photoperiod had no effect on BW or absolute abdominal fat weight at first egg. Results from the current study showed that photoperiod had no effect on BW and absolute abdominal fat, but the 16L:8D photoperiod group reduced ovary weight in chickens at first egg compared with the 12L:12D group. Feed restriction early in life has been proposed as a strategy for improving feed efficiency and reducing body fat in broilers (Akande Atteh, 2016Akande KE, Atteh JO. The influence of different regiments of early nutrient restriction on performance and abdominal fat of broilers. Journal of Animal Production Research 2016;28(1):189-195.; Xu et al., 2017Xu C, Yang H, Wang Z, Wan Y, Hou B, Ling C. The Effects of early feed restriction on growth performance, internal organs and blood biochemical indicators of broilers. Animal and Veterinary Sciences 2017;5(6):121.). Previous studies have shown that feed restriction (75% of control ad libitum) delayed the broilers age of sexual maturity and significantly reduced ovary weight, number of yellow follicles, number of atretic yellow follicle, incidence of double hierarchy, internal ovulation as compared to control from 19 to 25 wk of age (Madnurkar et al., 2014Madnurkar AD, Shinde AS, Chouhan L, Singh V, Mohan J, Moudgal RP. Effect of dietary phytoestrogens, feed restriction, and their interaction on reproductive status of broiler pullets. Veterinary World 2014;7(12):1041-1046.). During egg production, feed restriction resulted in significantly lower body and abdominal fat pad weights compared with unrestricted feeding (Richards et al., 2003Richards MP, Poch SM, Coon CN, Rosebrough RW, Ashwell CM, McMurtry JP. Feed restriction significantly alters lipogenic gene expression in broiler breeder chickens. The Journal of Nutrition 2003;133(3):707-715.). The data of the present study showed that feed restriction could reduce abdominal fat weight at the age of 14 wk and first egg, and there was an interaction effect between photoperiod and feed restriction on ovary weight at first egg. The age at first egg (AFE) was affected in a curviform by the lighting intensity and length of the photoperiod (Lewis et al., 1997Lewis PD, Perry GC, Morris TR. Effect of size and timing of photoperiod increase on age at first egg and subsequent performance of two breeds of laying hen. British Poultry Science 1997;38(2):142-150.). Exposure to photoperiods of 17L:7D, 15L:9D, 13L:11D or 11L:13D significantly affected the age at first egg (Chen et al., 2007). The average age at first egg was 144.8 d for the 17L:7D group and 150.5 d for the 11L:13D group. In the present study, the age of the first egg in the 16L:8D photoperiod group was 10.45 d earlier than in the 8L:16D photoperiod group. There was no interaction effect between photoperiod and food restriction on the age of the first egg and first egg weight. The current data further evidences that the photoperiod remains the primary mediator of regulating AFE in birds.

A study of Japanese quail in which leptin was injected in ovo enhanced the growth rate during embryonic and postembryonic development and led to earlier hatching and puberty (Lamosova et al., 2003Lamosova D, Macajova M, Zeman M, Mozes S, Jezova D. Effect of in ovo leptin administration on the development of Japanese quail. Physiological Research 2003;52(2):201-209.). Furthermore, whereas a single injection of leptin in chickens resulted in attenuation of feed intake (Cassy et al., 2004Cassy S, Picard M, Crochet S, Derouet M, Keisler DH, Taouis M. Peripheral leptin effect on food intake in young chickens is influenced by age and strain. Domestic Animal Endocrinology 2004;27(1):51-61.; Denbow et al., 2000Denbow DM, Meade S, Robertson A, McMurtry JP, Richards M, Ashwell C. Leptin-induced decrease in food intake in chickens. Physiology Behavoir 2000;69(3):359-362.; Lohmus et al., 2003Lohmus M, Sundstrom LF, El Halawani M, Silverin B. Leptin depresses food intake in great tits (Parus major). General and Comparative Endocrinology 2003;131(1):57-61.; Raver et al., 1998Raver N, Taouis M, Dridi S, Derouet M, Simon J, Robinzon B, Djiane J, Gertler A. Large-scale preparation of biologically active recombinant chicken obese protein (leptin). Protein Expression and Purification 1998;14(3):403-408.; Taouis et al., 2001Taouis M, Dridi S, Cassy S, Benomar Y, Raver N, Rideau N, et al. Chicken leptin:properties and actions. Domestic Animal Endocrinology 2001;21(4):319-327.), but not chronic leptin injections lasting several weeks. It is now clear that reproductive maturation will not take place in the complete absence of leptin signaling (i.e. in mammals lacking either functional leptin or its receptor) but leptin is not necessarily the rate-limiting determinant for puberty onset, it acts rather as a permissive factor or ‘metabolic gate’ (Foster Nagatani, 1999Foster DL, Nagatani S. Physiological perspectives on leptin as a regulator of reproduction:role in timing puberty. Biology Reproduction 1999;60(2):205-215.). For example, leptin will not advance the timing of normal puberty in ad libitum fed rats, but in moderately feed restricted prepubertal rats, puberty is delayed. This delay can be prevented by simultaneous treatment with leptin, leading to the result that puberty occurs at a similar time to ad-libitum fed rats (Cheung et al., 1997Cheung CC, Thornton JE, Kuijper JL, Weigle DS, Clifton DK, Steiner RA. Leptin is a metabolic gate for the onset of puberty in the female rat. Endocrinology 1997;138(2):855-858.). This study suggested that feed restriction significantly inhibited ovary LEPR gene expression at 14 wk, 18 wk and at first egg, but did not significantly affect abdominal fat LEPR gene expression at 18 wk and at first egg. The current data evidences that photoperiod mainly mediates the abdominal fat LEPR gene expression, while feed restriction mostly mediated the ovary LEPR gene expression.

In birds, melatonin binding sites have been identified in the ovaries, suggesting a possible role of melatonin regulating ovarian functions (Sundaresan et al., 2009Sundaresan NR, Marcus Leo MD , Subramani J, Anish D, Sudhagar M, Ahmed Ka, et al. Expression analysis of melatonin receptor subtypes in the ovary of domestic chicken. Veterinary Research Communications 2009;33(1):49-56.). The present findings are in line with the hypothesis that melatonin directly acts on the gonads (Ayre Pang, 1994Ayre EA, Pang SF. 2-[125I] iodomelatonin binding sites in the testis and ovary:putative melatonin receptors in the gonads. Neurosignals 1994;3(2):71-84.). In the current study, we observed two main subtypes of melatonin receptors expression in the ovary. The differential distribution of MELR1A and MELR1B in ovarian tissues suggests that these receptors mediate distinct downstream cellular functions of melatonin in these tissues. There was a trend towards feed restriction reducing ovary expression of LEPR and MELR1B mRNA in treated chicken.

The role of estrogens in hen reproduction has been well established (Hrabia et al., 2008Hrabia A, Wilk M, Rzasa J. Expression of alpha and beta estrogen receptors in the chicken ovary. Folia Biologica 2008;56(3-4):187-191.). Therefore, the mRNA expression of estrogen receptors under different photoperiod and feed restriction was examined within the ovaries of pullets. The current study showed that there was a trend towards feed restriction reducing ovary expression of ER mRNA in treated chickens, but photoperiod did not affect ER mRNA expression.

CONCLUSION

Taken together, the results of this study suggest that feed restriction down regulated the ER, LEPR, MELR1A and MELR1B mRNA expression of the ovary at 14 wk, 18 wk, and AFE. Long photoperiod enhanced the LEPR, MELR1A and MELR1B mRNA expression of abdominal fat at AFE. Moreover, a better understanding of the mechanisms governing the partitioning of leptin and melatonin between adipose and ovarian tissue were reached, thereby enabling strategies to effectively control the threshold of sexual maturation in chickens.

ACKNOWLEDGMENTS

This work was supported by the China Agriculture Research System [grant numbers CARS-41-K18].

REFERENCES

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  • Akande KE, Atteh JO. The influence of different regiments of early nutrient restriction on performance and abdominal fat of broilers. Journal of Animal Production Research 2016;28(1):189-195.
  • Ayre EA, Pang SF. 2-[125I] iodomelatonin binding sites in the testis and ovary:putative melatonin receptors in the gonads. Neurosignals 1994;3(2):71-84.
  • Bouloumie A, Drexler HC, Lafontan M, Busse R. Leptin, the product of Ob gene, promotes angiogenesis. Circulation Research 1998;83(10):1059-1066.
  • Bozkurt M, Ayhan V, Kirkpinar F. The effects of different qualitative and quantitative feed restriction methods during rearing on the reproductive performance of broiler breeder hens. Revue De Médecine Vétérinaire 2014;163(8):405-410.
  • Brecchia G, Bonanno A, Galeati G, Federici C, Maranesi M, Gobbetti A, et al. Hormonal and metabolic adaptation to fasting:effects on the hypothalamic-pituitary-ovarian axis and reproductive performance of rabbit does. Domestic Animal Endocrinology 2006;31(2):105-122.
  • Brody T, Eitan Y, Soller M, Nir I, Nitsan Z. Compensatory growth and sexual maturity in broiler females reared under severe food restriction from day of hatching. British Poultry Science 1980;21(6):437-446.
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  • Chen H, Huang RL, Zhang HX, Di KQ, Pan D, Hou YG. Effects of photoperiod on ovarian morphology and carcass traits at sexual maturity in pullets. Poultry Science 2007;86(5):917-920.
  • Cheung CC, Thornton JE, Kuijper JL, Weigle DS, Clifton DK, Steiner RA. Leptin is a metabolic gate for the onset of puberty in the female rat. Endocrinology 1997;138(2):855-858.
  • Crouch AN, Grimes JL, Christensen VL, Krueger KK. Effect of physical feed restriction during rearing on Large White turkey breeder hens:2. reproductive performance. Poultry Science 2002;81(1):16-22.
  • De Beer M, Coon CN. The effect of different feed restriction programs on reproductive performance, efficiency, frame size, and uniformity in broiler breeder hens. Poultry Science 2007;86(9):1927-1939.
  • Denbow DM, Meade S, Robertson A, McMurtry JP, Richards M, Ashwell C. Leptin-induced decrease in food intake in chickens. Physiology Behavoir 2000;69(3):359-362.
  • Fantuzzi G, Faggioni R. Leptin in the regulation of immunity, inflammation, and hematopoiesis. Journal of Leukocyte Biology 2000;68(4):437-446.
  • Foster DL, Nagatani S. Physiological perspectives on leptin as a regulator of reproduction:role in timing puberty. Biology Reproduction 1999;60(2):205-215.
  • Hocking PM. Roles of body weight and feed intake in ovarian follicular dynamics in broiler breeders at the onset of lay and after a forced molt. Poultry Science 2004;83(12):2044-2050.
  • Horev G, Einat P, Aharoni T, Eshdat Y, Friedman-Einat M. Molecular cloning and properties of the chicken leptin-receptor (CLEPR) gene. Molecular and Cellular Endocrinology 2000;162(1-2):95-106.
  • Hrabia A, Wilk M, Rzasa J. Expression of alpha and beta estrogen receptors in the chicken ovary. Folia Biologica 2008;56(3-4):187-191.
  • Huber-Eicher, B, Suter, A, Spring-Stã¤Hli, P, 2013. Effects of colored light-emitting diode illumination on behavior and performance of laying hens. Poult Sci,92(4):869-873.
  • Lamosova D, Macajova M, Zeman M, Mozes S, Jezova D. Effect of in ovo leptin administration on the development of Japanese quail. Physiological Research 2003;52(2):201-209.
  • Lewis PD, Danisman R, Gous, RM. Photoperiods for broiler breeder females during the laying period. Poultry Science 2010:89(1):108.
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  • Liu X, Dunn IC, Sharp PJ, Boswell T. Molecular cloning and tissue distribution of a short form chicken leptin receptor mRNA. Domestic Animal Endocrinology 2007;32(3):155-166.
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  • Lohmus M, Sundstrom LF, El Halawani M, Silverin B. Leptin depresses food intake in great tits (Parus major). General and Comparative Endocrinology 2003;131(1):57-61.
  • Madnurkar AD, Shinde AS, Chouhan L, Singh V, Mohan J, Moudgal RP. Effect of dietary phytoestrogens, feed restriction, and their interaction on reproductive status of broiler pullets. Veterinary World 2014;7(12):1041-1046.
  • Malpaux B, Migaud M, Tricoire H, Chemineau P. Biology of mammalian photoperiodism and the critical role of the pineal gland and melatonin. Journal Biological Rhythms 2001;16(4):336-347.
  • Paczoska-Eliasiewicz HE, Proszkowiec-Weglarz M, Proudman J, Jacek T, Mika M, Sechman A, et al. Exogenous leptin advances puberty in domestic hen. Domestic Animal Endocrinology 2006;31(3):211-226.
  • Pitel F, Faraut T, Bruneau G, Monget P. Is there a leptin gene in the chicken genome? Lessons from phylogenetics, bioinformatics and genomics. General and Comparativo Endocrinology 2010;167(1):1-5.
  • Proudfoot FG. Effect of rearing and adult feed restriction and photoperiod regimens on the performance of four meat parent chicken genotypes. Canadian Journal of Animal Science 1979;59(4):749-759.
  • Raver N, Taouis M, Dridi S, Derouet M, Simon J, Robinzon B, Djiane J, Gertler A. Large-scale preparation of biologically active recombinant chicken obese protein (leptin). Protein Expression and Purification 1998;14(3):403-408.
  • Richards MP, Poch SM, Coon CN, Rosebrough RW, Ashwell CM, McMurtry JP. Feed restriction significantly alters lipogenic gene expression in broiler breeder chickens. The Journal of Nutrition 2003;133(3):707-715.
  • Schweanlardner,K, Fancher BI, Classen HL. Impact of daylength on the productivity of two commercial broiler strains. British Poultry Science 2012;53(1):7-18.
  • Sinkalu VO, Ayo, JO, Abimbola AA, Ibrahim, JE. Effects of melatonin on cloacal temperature and erythrocyte osmotic fragility in layer hens during the hot-dry season. Journal of Applied Animal Research 2015;43(1):52-60.
  • Sirotkin AV, Grossmann R. Interrelationship between feeding level and the metabolic hormones leptin, ghrelin and obestatin in control of chicken egg laying and release of ovarian hormones. Comparative Biochemistry and Physiology Part A:Molecular & Integrative Physiology 2015;184(1-5).
  • Sundaresan NR, Marcus Leo MD , Subramani J, Anish D, Sudhagar M, Ahmed Ka, et al. Expression analysis of melatonin receptor subtypes in the ovary of domestic chicken. Veterinary Research Communications 2009;33(1):49-56.
  • Taouis M, Chen JW, Daviaud C, Dupont J, Derouet M, Simon J. Cloning the chicken leptin gene. Gene 1998;208(2):239-242.
  • Taouis M, Dridi S, Cassy S, Benomar Y, Raver N, Rideau N, et al. Chicken leptin:properties and actions. Domestic Animal Endocrinology 2001;21(4):319-327.
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Publication Dates

  • Publication in this collection
    11 Nov 2019
  • Date of issue
    2019

History

  • Received
    13 Mar 2019
  • Accepted
    26 June 2019
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